REGULAR PAPER
HISTOLOGY OF THE ILEUM IN BEES
(HYMENOPTERA, APOIDEA)
Carolina Gonçalves Santos and José Eduardo Serrão
Department of General Biology, Federal University of Viçosa (UFV), Viçosa, MG, Brazil.
ABSTRACT
In most hymenopterans, the ileum extends as a long tube from the midgut to the rectum, and shows no
marked anatomical specialization. The function of the ileum is not fully understood, although the presence
of an epithelial layer of cuboidal or columnar cells with apical and basal plasma membrane infoldings
suggests that this organ may be involved in water and nutrient absorption. In this work, we investigated
the ileal morphology of 47 species of bees in the Andrenidae, Apidae (Apini, Meliponini, Xylocopinae,
Centridini, Bombini, Eucerini, Euglossini, Tapinotaspidini, Exomalopsini), Halictidae and Megachilidae,
as part of a study to understand the physiological and phylogenetic importance of this organ. In all cases,
the ileum consisted of an epithelium containing cuboidal or columnar cells that usually had basal nuclei and
apical plasma membrane infoldings, although there were variations in cell shape, position of the nucleus,
degree of chromatin condensation and cuticle thickness. The epithelial cells were covered with a cuticle and
transverse sections revealed the presence of 4-6 folds projecting into the lumen. The cell cytoplasm below
the apical plasma membrane infoldings contained numerous vacuoles of different sizes. A single layer of
circular muscle was located beneath the epithelium. The histological organization of the ileum suggested
a role in the absorption of luminal solutes as a mechanism for regulating the hemolymph and the general
osmotic balance of these insects. However, there was no relationship between the structural organization of
the ileum and the degree of social development and/or phylogeny of the bees.
Key words: Digestive tract, morphology, osmotic control, physiology
INTRODUCTION
The digestive tract of insects is divided into
foregut, midgut and hindgut. The foregut and the
hindgut are of ectodermal origin whereas the midgut
is endodermic [6]. In bees, the foregut consists of
the pharynx, esophagus, crop and proventriculus, the
midgut corresponds to the ventriculus and the hindgut
is divided into ileum and rectum [3,4,10,22,34,39].
Various morphological and biochemical aspects of
the digestive tract of bees have been studied [7,13,1517,23,25,29,32,41]. However, the ileum had received
less attention because of the general belief that the
midgut is responsible for food digestion and nutrient
absorption whereas the rectum is responsible for
osmotic control [32,35-37].
The ileum of bees is a long tube interposed between
the midgut and the rectum but shows no visible
(macroscopic) anatomical specialization throughout
_______________
Correspondence to: Dr. José Eduardo Serrão
Departamento de Biologia Geral, Universidade Federal de Viçosa (UFV),
CEP: 36570000, Viçosa, MG, Brazil. Tel: (55) (31) 3899-1301, Fax: (55)
(31) 3899-2549. E-mail: [email protected]
its length. Although its precise function remains to be
established, the ileum may be involved in water and
nutrient absorption [8]. In the stingless bee Melipona
quadrifasciata anthidiodes, the epithelial cells of the
ileum have four types of microvilli, indicating that
there may be some form of compartmentalization
in the absorption of organic solutes; this finding,
together with other ultrastructural features, is also
suggestive of a digestive function [9,10].
Morphological variations in the digestive tract
of insects have been related to differences in their
feeding habits and degree of sociality [1,4,11,12,18].
However, phylogenetic relationships may also
influence insect gut morphology [29,32,33,42]. In this
context, studies designed to compare the histological
structure of the ileum in different species of bees are
required to test the hypothesis that variations in this
organ are related to phylogeny and/or the degree of
sociality in these insects. The purpose of this study
was to compare the histology of the ileum in bees
belonging to several tribes of four families in order
to assess the foregoing relationships.
Braz. J. morphol. Sci. (2006) 23(3-4), 405-413
406
C. G. Santos and J. E. Serrão
MATERIAL AND METHODS
Forty-seven species of bees from the Andrenidae, Apidae
(Apini, Meliponini, Xylocopinae, Centridini, Bombini,
Eucerini, Euglossini, Tapinotaspidini, Exomalopsini),
Halictidae and Megachilidae were studied (Table 1). The
bees were collected while foraging on flowers in the towns
of Viçosa (Minas Gerais state) and Boituva (São Paulo
state) and transported to the laboratory where they were
killed by freezing. The bees were subsequently dissected
using a stereomicroscope and the digestive tract was
removed, immersed in insect saline solution (0.1 M NaCl,
0.1 M Na2HPO4, 0.1 M KH2PO4) and then transferred to
Zamboni solution [40] for 4 h. After fixation, the hindgut
was isolated and the length of the ileum was measured
using a micrometer eyepiece (Olympus).
For histological analysis, the tissues were dehydrated
in an ethanol series, embedded in glycol metacrylate (JB4
EMS historesin, Warrington, PA, USA), sectioned into 4μm-thick sections and stained with hematoxylin and eosin
(HE). The Feulgen reaction was done to identify nuclear
DNA [24]. The thickness of the cuticle lining the lumen of
the ileum was measured with a micrometer eyepiece. After
fixation and dehydration, another set of ilea was transferred
to hexamethyldisilazane for 5 min, air dried, sputtered with
gold, and examined with a LEO VP1430 scanning electron
microscope operated at 15 kV.
The size of the bees was determined by measuring
the intertegular distance (distance between the forewing
tegulae) [5] with a micrometer eyepiece. The morphometric
data for 30 species (Table 2) were analyzed by analysis
of covariance (ANCOVA) to determine the correlation
between body size, ileal length and degree of sociality.
RESULTS
The ileum corresponded to the proximal portion
of the hindgut, with the transition from the distal
midgut to the ileum being marked by a valve located
just above the opening of the Malpighian tubules (Fig.
1A,B). The ileal lumen was lined by a cuticle that
extended throughout its entire length and included
the rectum (Fig. 1C,D). The posterior distal region of
the ileum protruded into the rectum where it formed
a valve-like structure (Fig. 1C). Transverse sections
showed that the epithelium consisted of 4-6 folds
that bulged into the lumen (Fig. 2A). Externally,
there was a single layer of circular muscle formed
by several muscle fibers (Fig. 2C,D), and interposed
between this layer and the ileal epithelium was a
distinct subepithelial space that was larger at the base
of the epithelial folds where the muscle layer was
interrupted to allow entrance of the tracheae (Fig.
Braz. J. morphol. Sci. (2006) 23(3-4), 405-413
2B). The single layered epithelium consisted of only
one cell type that varied from cuboidal to columnar.
All of the specimens examined had flattened cells
at the ileal-rectal interface (Fig. 1C), with the
ileal epithelial cells usually having apical plasma
membrane infoldings and basal nuclei (Fig. 3A).
Although the structural organization of the ileal wall
was similar in all of the species examined here, there
were some variations in epithelial cell shape, position
of the nucleus, degree of chromatin condensation and
cuticular thickness. Thus, for example, Apis mellifera,
Cephalotrigona capitata, Exomalopsis auropilosa,
Melipona rufiventris, M. compressipes, M. eburnea,
Nannotrigona testaceicornis, Partamona helleri,
Paratrigona lineata, Plebeia remota, and Tetrapedia
nigritarsis had cuboidal epithelial cells (Fig. 3A,B)
while the other species had columnar cells (Figs. 3C,D
and 4A,C).
The cuticle that lined the epithelium throughout
its entire length varied in thickness from 0.7 μm to
4.6 μm in M. scutellaris and Xylocopa frontalis,
respectively (Table 2). In the epithelial cells of
Augochloropsis sp., Melipona capixaba and M.
scutellaris, the nucleus was located centrally (Fig.
3C), while in the other species it was located in the
basal portion of the cells (Fig. 4A). In Augochloropsis
sp., Bombus morio, Centris violacea, Epicharis flava,
Euglossa mandibularis, Exomalopsis auropilosa,
Friesomelitta varia, Geotrigona sp., Megachile spp.,
Megalopta sp., Paratrigona lineata and Xylocopa
frontalis the chromatin was decondensed (Figs. 3D
and 4A,B), although in many other species some
regions of condensed chromatin were seen (Figs.
3A-C and 4C). The Feulgen reaction showed that the
nucleus had many regions of condensed chromatin,
with the cytoplasm containing numerous vacuoles
of different sizes, the presence of which deformed
the nucleus (Figs. 3A,B and 4B,C). These vacuoles
occurred throughout the entire length of the ileum,
except in A. mellifera, E. mandibularis, F. varia,
Melipona quadrifasciata anthidioides, M. bicolor
and P. helleri, in which they accumulated in the
posterior half of the organ. Apical plasma membrane
infoldings that reached the medium portion of the
cell were also observed (Fig. 3A).
The size of the ileum generally increased with body
size (Table 2) (ANCOVA: F1.27 = 64.39; p < 0.001),
but there was no relationship with the degree of sociality
(ANCOVA: F1.27 = 0.86; p < 0.361) (Fig. 5).
407
Histology of the ileum in bees
Table 1. List of the taxa studied.
Family
Tribe
Species
Apidae
Apini
Meliponini
Apis mellifera Linnaeus, 1758
Cephalotrigona capitata (Smith, 1854)
Frieseomelitta flavicornis (Fabricius, 1798)
Frieseomelitta varia (Lepeletier, 1836)
Geotrigona sp.
Lestrimelitta limao (Smith, 1836)
Melipona asilvai (Moure, 1971)
Melipona bicolor (Lepeletier, 1836)
Melipona capixaba (Moure & Camargo,1995)
Melipona compressipes (Fabricius,1804)
Melipona eburnea (Friese, 1900)
Melipona quadrifasciata anthidiodes (Lepeletier, 1836)
Melipona quinquefasciata (Lepeletier, 1836)
Melipona rufiventris (Lepeletier 1836)
Melipona scutellaris (Latreille, 1811)
Nannotrigona testaceicornis (Lepeletier, 1836)
Paratrigona lineata (Lepeletier, 1836)
Paratrigona subnuda (Moure, 1947)
Partamona helleri (Friese, 1900)
Plebeia remota (Holmberg, 1903)
Ptilotrigona sp.
Scaptotrigona postica (Latreille, 1807)
Trigona spinipes (Fabricius, 1793)
Bombus atratus (Franklin, 1913)
Bombus morio (Swederus, 1787)
Eufriesea violacea (Blanchard, 1840)
Euglossa (Glossura) imperialis (Cockerell, 1922)
Euglossa mandibularis
Eulaema nigrita (Lepeletier, 1841)
Exaerete smaragdina (Guérin-Méneville, 1845)
Xylocopa frontalis (Oliver,1789)
Xylocopa (Schoenherria) subcyanea (Perez,1901)
Centris violacea (Lepeletier, 1841)
Epicharis flava (Friese, 1900)
Thygater analis (Lepeletier, 1841)
Thygater palliventris (Friese, 1908)
Exomalopsis auropilosa (Spinola, 1853)
Tetrapedia nigritarsis (Moure & Mucci, 1998)
Augochlora sp.
Augochloropsis sp.
Megalopta sp.
Pseudaugochlora gramínea (Fabricius, 1804)
Rhinocorynura briseis (Smith, 1853)
Oxaea flavescens (Klug, 1807)
Megachile aureiventris (Schrottky, 1902)
Megachile (Leptorachis) paulistana (Schrottky, 1902)
Megachile (Cressoniella) rava (Vachal, 1808)
Bombini
Euglossini
Xylocopini
Centridini
Apidae
Eucerini
Halictidae
Exomalopsini
Tapinotaspidini
Augochlorini
Andrenidae
Megachilidae
Oxaeini
Megachilini
Braz. J. morphol. Sci. (2006) 23(3-4), 405-413
408
C. G. Santos and J. E. Serrão
Table 2. Length, cuticular thickness and intertegular distance of the ileum in bees.
Species
Apidae
Apis mellifera
Cephalotrigona capitata
Frieseomelitta varia
Geotrigona sp.
Lestrimelitta limao
Melipona eburnea
Melipona quadrifasciata anthidiodes
Melipona rufiventris
Melipona scutellaris
Paratrigona lineata
Paratrigona subnuda
Partamona helleri
Ptilotrigona sp.
Scaptotrigona postica
Trigona spinipes
Bombus atratus
Bombus morio
Eufriesea violacea
Euglossa (Glossura) imperialis
Eulaema nigrita
Exaerete smaragdina
Xylocopa frontalis
Xylocopa (Schoenherria) subcyanea
Centris violacea
Epicharis flava
Halictidae
Augochlora sp.
Andrenidae
Oxaea flavescens
Megachilidae
Megachile aureiventris
Megachile (Leptorachis) paulistana
Megachile (Cressoniella) rava
DISCUSSION
The presence of a single layer of circular muscle
in the species of Apoidea investigated here differed
from that in some species of Lepidoptera, which
have two muscle layers (external circular and inner
longitudinal muscles) [20] and Coleoptera, in which
the inner muscle layer is circular and the external layer
is longitudinal [38]. The presence of a single layer of
circular muscle has also been reported in ants [43].
These findings indicate that the ileum has a uniform
structure within the Hymenoptera, although additional
studies in wasps are necessary to confirm this.
A comparison of the variations in ileal structure
with the phylogeny of bees, as previously done by
Braz. J. morphol. Sci. (2006) 23(3-4), 405-413
Ileum
(mm)
Intertegular distance
(mm)
Cuticular thickness
(μm)
3.66
1.85
0.77
1.27
1.13
4.25
5.03
3.61
6.57
0.66
0.64
1.75
1.94
2.13
1.74
11.92
13.58
6.83
6.46
11.17
8.23
15.64
3.26
6.26
12.85
3.00
2.11
1.24
1.61
1.62
3.08
3.45
2.55
2.73
1.18
1.00
1.93
1.48
1.91
1.71
4.24
4.55
4.45
3.52
5.59
4.43
7.82
3.14
5.20
4.90
1.40
1.56
2.46
2.20
2.88
2.52
2.08
1.20
0.70
1.96
3.92
2.92
3.48
4.52
2.17
1.10
1.96
1.96
4.60
4.30
3.16
2.48
1.24
1.63
2.36
7.06
6.17
2.28
3.54
1.87
3.12
3.50
2.60
2.63
1.68
2.08
2.50
Roig-Alsina and Michener [31], Peixoto and Serrão
[29] and Serrão [33] for other characteristics, revealed
no relationship between these two parameters, which
suggested that the ileum is not a useful character for
phylogenetic analyses in bees.
The main function of the insect hindgut is
to modify the composition of the primary urine
produced by the Malpighian tubules by releasing
K+, Na+ and Cl- into the lumen, thereby promoting
the influx of water and of substances to be excreted
[6]. This modification occurs mainly in the rectum
but apparently begins in the ileum, which is efficient
in absorbing water and ions, and in regulating acidbase balance and nitrogen excretion [14,19,30]. The
Histology of the ileum in bees
409
Figure 1. A. Section of the ileum of Melipona eburnea showing the transition from midgut (Mg) to ileum (IL) and the pyloric
valve (PV). Arrowheads - Malpighian tubules, M - muscle. Bar = 50 μm. B. Detail of the pyloric valve (PV) in the ileum (IL)
of Eufriesea violacea. L - lumen, M – muscle, Mg - midgut. Bar = 30 μm. C. Transition area from the ileum (IL) to the rectum
(R) in Bombus morio showing the columnar cells (large arrow) becoming flattened (small arrow). L - lumen. Bar = 40 μm.
D. Scanning electron micrograph of the ileal lumen of Melipona quadrifasciata anthidioides showing the cuticle (C) that lines
the organ. Mp - peritrophic membrane. Bar = 100 μm.
Figure 2. A. Transverse section of the ileum of Thygater palliventris showing the epithelial folds and the layer of circular
muscle (M). Arrow - nucleus of epithelial cell, arrowhead - cuticle, L - lumen. Bar = 50 μm. B. Detail of the ileum of
Eufriesea violacea showing the muscular layer (M) interrupted by the entrance of tracheae (arrowhead). C - cuticle, L –
lumen, Nu – nucleus. Bar = 40 μm. C. Scanning electron micrograph of the ileum of Melipona quadrifasciata anthidioides
showing the layer of circular muscle fibers (M) that surrounds the organ. Arrow - epithelium of the ileum, Tr - trachea.
Bar = 20 μm. D. Scanning electron micrograph of the ileum of Apis mellifera showing a detail of the circular muscles (M).
Part of the cuticle (C) that covers the epithelium of the organ internally can be seen. Tr - trachea. Bar = 20 μm.
Braz. J. morphol. Sci. (2006) 23(3-4), 405-413
410
C. G. Santos and J. E. Serrão
Figure 3. A. The ileum of Melipona eburnea showing the epithelium with cuboidal cells and the apical plasma membrane
infoldings (arrowheads) extending to the middle portion of the cell. C - cuticle, L - lumen, M - muscles, Nu - nucleus,
Va - vacuoles. Bar = 10 μm. B. The ileum of Cephalotrigona capitata showing the epithelium with cuboidal cells, basal
nucleus (Nu) and condensed chromatin (arrowheads). Note the apical plasma membrane infoldings (arrows) and large
vacuoles (Va). C - cuticle, L - lumen. Bar = 10 μm. C. The ileum of Melipona capixaba showing the centrally located
nucleus (Nu) of the epithelial cells and the condensed chromatin (arrows). The arrowheads indicate the apical plasma
membrane infoldings. C - cuticle, L - lumen. Bar = 10 μm. D. The ileum of Bombus morio showing the epithelium with
columnar cells and thick cuticle (C). The arrows show the apical plasma membrane infoldings. Arrowheads - chromatin
condensed, L - lumen, Nu - nucleus. Bar = 10 μm.
Figure 4. A. The ileum of Centris violacea showing the epithelium with columnar cells, basal nucleus (Nu) and
decondensed chromatin (arrowhead). Note the presence of vacuoles (arrows) in the cytoplasm. C - cuticle, L - lumen.
Bar = 10 μm. B. The ileum of Megachile (Cressoniella) rava showing the epithelium and nuclei containing decondensed
chromatin (Nu). Note that the nuclear shape is distorted by the accumulation of vacuoles (Va). Arrow - basal lamina,
Tr – trachea. Bar = 10 μm. C. The ileum of Eulaema nigrita showing deformations of the nucleus (Nu) caused by large
vacuoles (Va) in the cytoplasm. Arrowhead - condensed chromatin, C - cuticle, L - lumen. Bar = 10 μm.
Braz. J. morphol. Sci. (2006) 23(3-4), 405-413
411
Histology of the ileum in bees
16
Length of the ileum (mm)
14
12
10
8
6
4
2
0
0
1
2
3
4
5
6
7
8
9
Intertegular distance (mm)
Figure 5. Analysis of covariance (ANCOVA) showing the relationship between ileal length, bee size (intertegular distance)
and the degree of sociality in the species studied. O - solitary bees, ò - social bees.
presence of apical plasma membrane infoldings and
the accumulation of vacuoles within the cells seen in
the bees studied here suggest that the ileum plays a role
in nutrient absorption. This conclusion agrees with the
classic function of the ileum in modifying the primary
urine produced by the Malpighian tubules [43].
The primary urine that arrives in the ileum is
isosmotic compared to hemolymph, but its volume
and concentration decrease and increase, respectively,
during transit through the ileum, via a process that is
dependent on active ion pumping into the epithelial
cells [2]. The presence of basal and apical folds in the
ileal epithelium is compatible with this view since
this specialization is typical of epithelia involved
in active transport. However, in insects that feed on
nectar, the primary urine is hypo-osmotic compared
to hemolymph [26,27]. Xylocopa capitata bees have
a moderately concentrated hemolymph and dilute
urine, and because of the low level of ions they ingest
these bees need to conserve ions rather than water in
order not to suffer water stress [27]. In the butterfly
Pieris brassicae, the filtrate that arrives in the
ileum from the Malpighian tubules is hypo-osmotic
compared to hemolymph and there is a decrease in
the K+ concentration of the primary urine as it passes
through the ileum, thereby ensuring that enough K+
remains in the hemolymph to support fluid secretion
by the Malpighian tubules [26]. These findings
indicate that, in the absence of an osmotic gradient,
there may be ion absorption without water flow.
Since bees feed on nectar, it is reasonable to
suppose that the primary urine of these insects is
hypo-osmotic compared to hemolymph. Hence, to
maintain their osmotic balance, bees need to absorb
ions from the primary urine without a corresponding
water flow. Such minimal coupling between solute
and water transport has been observed in the salivary
glands of Calliphora erythocephala (Diptera) and in the
Malpighian tubules of Rhodnius praliocus (Hemiptera),
both of which produce hypo-osmotic fluids by ion
resorption from an initially isosmotic secretion [21,28].
In Pieris brassicae, K+ is reabsorbed passively by the
ileum and the low water permeability of this epithelium
maintains the osmotic gradient [26].
The morphological aspects of the ileum in
described here, such as the infolding of the apical
plasma membrane and the presence of vacuoles in
the basal region of these cells are indicative of solute
absorption without water flow. In a hypothetical
model of this physiological mechanism, solutes
would be absorbed from the ileal lumen and stored
temporarily inside vacuoles, thereby avoiding the
influx of water that would dilute the hemolymph and
alter the osmotic balance in these insects.
Braz. J. morphol. Sci. (2006) 23(3-4), 405-413
412
C. G. Santos and J. E. Serrão
In conclusion, the results of this study indicate that
although the ileum of bees present some variations
among species, this organ has not relationships with
the sociality degree and phylogeny of bees being
its morphological features related with the osmotic
control in all species of bees studied.
ACKNOWLEDGMENTS
The authors thank anonymous referees whose critical
reading and suggestions improved the final version of this
manuscript. This work was supported by the Conselho
Nacional de Desenvolvimento Científico e Tecnológico
(CNPq) and the Fundação de Amparo à Pesquisa do Estado
de Minas Gerais (FAPEMIG).
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______________
Received: April 3, 2006
Accepted: August 4, 2006
Braz. J. morphol. Sci. (2006) 23(3-4), 405-413